Long time ago, two gods, Bardus and Octum, fought for dominance in the world. The benevolent Bardus defeated the evil Octum, but as a result has lost his power and had to be dissected into six parts, which were since watched over by the goddess Durga.

Many years later, two young people - Avin and his sister Eimelle - are working for the Church of Bardus. One day a mysterious man who calls himself Belias arrives and murders Avin's old mentor. The two youths embark on a journey to find the murderer and eventually discover the truth about their own role in events that will decide the fate of the world...

Akai Shizuku mostly relies on the Japanese RPG template gameplay-wise, having linear plot progression, emphasis on story and characters, automatic leveling, etc. There is no "world map", but a continuous world in which important locations are connected by many "empty" areas. Combat system builds upon that of the predecessor, also allowing the player to let the characters fight automatically; however, it offers more control over the characters' actions, including precise moving on the battle field. Enemies appear at pre-set locations. Characters use physical attacks, offensive and healing magic, and can also summon creatures to help them in battle.